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Discovery of rim region between core and surface of proteins

Amal Kumar Bandyopadhyay
Department of Biotechnology, The University of Burdwan, Burdwan, West Bengal, India

Sahini Banerjee
Department of Biological Sciences, Indian Statistical Institute, Kolkata, West Bengal, India

Somnath Das
Department of Education, CDOE, The University of Burdwan, West Bengal, India

Published online:30th November, 2024

DOI: https://doi.org/10.52756/lbsopf.2024.e03.003

Keywords: Rim-region, topological pattern, interior cavity, non-bonded interaction, protein compaction

Abstract:

The crystal structure reveals the complexities of protein component organization from the core to the surface. In general, the existence of core and surface in protein structure is well known. Here, we raise the question of how this core and surface, respectively, end and begin. To further understand the concerns, we did a comprehensive investigation on high-resolution structures of three protein families [ADH (Alcohol Dehydrogenase), Glyceraldehyde 3-Phosphate Dehydrogenase (GDH), and Malate Dehydrogenase (MDH)] from various domains of life utilizing authentic methods. The results demonstrate the presence of a zone (designated as the rim), which has separate properties from the core and the surface.  The Kyte Doolittle grand average hydrophobicity (KD) of the core, surface, and rim are positive, negative, and neutral, respectively. Compared to the rim-zone, the core and surface have more hydrophobic residues and beta-strand structure, and charged residues and coil structure, respectively. In terms of polar residues and helix structure, compared to the rim, the core and surface have essentially similar but lower contents. The core’s long β-sheets and shell-water-filled cavities may restrict residue compaction in this location. These analyses, thus, demonstrate that the archaea employed a distinct approach to fine-tune the compaction of their core compared to the bacteria and eukaryotes. Simultaneously, the dominance of the coil at the surface appears to produce a similar result. Overall, our study provides evidence that the rim-zone has a very distinct structure from the core and surface. The study that applies to other proteins finds application in protein structure bioinformatics.

References:

  • Agashe, V. R., Shastry, M. C. R., & Udgaonkar, J. B. (1995). Initial hydrophobic collapse in the folding of barstar. Nature, 377(6551), 754-757. https://doi.org/10.1038/377754a0
  • Anfinsen, C. B. (1973). Principles that govern the folding of protein chains. Science, 181(4096), 223-230. https://doi.org/10.1126/science.181.4096.223
  • Baker, E. N., & Hubbard, R. E. (1984). Hydrogen bonding in globular proteins. Progress in biophysics and Molecular Biology, 44(2), 97-179. https://doi.org/10.1016/0079-6107(84)90007-5
  • Bandyopadhyay, A. K., & Sonawat, H. M. (2000). Salt dependent stability and unfolding of [Fe2-S2] ferredoxin of Halobacterium salinarum: spectroscopic investigations. Biophysical journal, 79(1), 501-510. https://doi.org/10.1016/S0006-3495(00)76312-0
  • Bandyopadhyay, A. K., Islam, R. N. U., & Hazra, N. (2020). Salt-bridges in the microenvironment of stable protein structures. Bioinformation, 16(11), 900. https://doi.org/10.6026/97320630016900
  • Bandyopadhyay, A. K., Islam, R. N. U., Mitra, D., Banerjee, S., & Goswami, A. (2019). Structural insights from water-ferredoxin interaction in mesophilic algae and halophilic archaea. Bioinformation, 15(2), 79. https://doi.org/10.6026/97320630015079
  • Bandyopadhyay, A. K., Islam, R. N. U., Mitra, D., Banerjee, S., & Goswami, A. (2019). Stability of buried and networked salt-bridges (BNSB) in thermophilic proteins. Bioinformation, 15(1), 61. https://doi.org/10.6026/97320630015061
  • Bandyopadhyay, A. K., Islam, R. N. U., Mitra, D., Banerjee, S., Yasmeen, S., & Goswami, A. (2019). Insights from the salt bridge analysis of malate dehydrogenase from H. salinarum and E. coli. Bioinformation, 15(2), 95. https://doi.org/10.6026/97320630015095
  • Bandyopadhyay, A. K., Krishnamoorthy, G., & Sonawat, H. M. (2001). Structural stabilization of [2Fe-2S] ferredoxin from Halobacterium salinarum. Biochemistry, 40(5), 1284-1292. https://doi.org/10.1021/bi001614j
  • Bandyopadhyay, A. K., Krishnamoorthy, G., Padhy, L. C., & Sonawat, H. M. (2007). Kinetics of salt-dependent unfolding of [2Fe–2S] ferredoxin of Halobacterium salinarum. Extremophiles, 11, 615-625. https://doi.org/10.1007/s00792-007-0075-0
  • Banerjee, S., Gupta, P. S. S., Islam, R. N. U., & Bandyopadhyay, A. K. (2021). Intrinsic basis of thermostability of prolyl oligopeptidase from Pyrococcus furiosus. Scientific Reports, 11(1), 11553. https://doi.org/10.1038/s41598-021-90723-4
  • Banerjee, S., Gupta, P. S. S., Nayek, A., Das, S., Sur, V. P., Seth, P., … & Bandyopadhyay, A. K. (2015). PHYSICO2: an UNIX based standalone procedure for computation of physicochemical, window-dependent and substitution based evolutionary properties of protein sequences along with automated block preparation tool, version 2. Bioinformation, 11(7), 366. https://doi.org/10.6026/97320630011366
  • Banerjee, S., Mondal, B., Islam, R. N. U., Gupta, P. S. S., Mitra, D., & Bandyopadhyay, A. (2018). POWAINDv1. 0: A Program for Protein-Water Interactions Determination. Bioinformation, 14(9), 530. https://doi.org/10.6026/97320630014530
  • Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., … & Bourne, P. E. (2000). The protein data bank. Nucleic Acids Research, 28(1), 235-242. https://doi.org/10.1093/nar/28.1.235
  • Betts, M. J., & Russell, R. B. (2003). Amino acid properties and consequences of substitutions. Bioinformatics for geneticists, 289-316. https://doi.org/10.1002/0470867302.ch14
  • Biswas, I., Mitra, D., Bandyopadhyay, A. K., & Mohapatra, P. K. D. (2020). Contributions of protein microenvironment in tannase industrial applicability: An in-silico comparative study of pathogenic and non-pathogenic bacterial tannase. Heliyon, 6(11). https://doi.org/10.1016/j.heliyon.2020.e05359
  • Bolon, D. N., & Mayo, S. L. (2001). Polar residues in the protein core of Escherichia coli thioredoxin are important for fold specificity. Biochemistry, 40(34), 10047-10053. https://doi.org/10.1021/bi010427y
  • Bottini, S., Bernini, A., De Chiara, M., Garlaschelli, D., Spiga, O., Dioguardi, M., … & Niccolai, N. (2013). ProCoCoA: a quantitative approach for analyzing protein core composition. Computational biology and chemistry, 43, 29-34. https://doi.org/10.1016/j.compbiolchem.2012.12.007
  • Ceccarelli, C., Liang, Z. X., Strickler, M., Prehna, G., Goldstein, B. M., Klinman, J. P., & Bahnson, B. J. (2004). Crystal structure and amide H/D exchange of binary complexes of alcohol dehydrogenase from Bacillus stearothermophilus: insight into thermostability and cofactor binding. Biochemistry, 43(18), 5266-5277. https://doi.org/10.1021/bi049736p
  • Dalhus, B., Saarinen, M., Sauer, U. H., Eklund, P., Johansson, K., Karlsson, A., … & Eklund, H. (2002). Structural basis for thermophilic protein stability: structures of thermophilic and mesophilic malate dehydrogenases. Journal of Molecular Biology, 318(3), 707-721. https://doi.org/10.1016/S0022-2836(02)00050-5
  • Dill, K. A. (1990). Dominant forces in protein folding. Biochemistry, 29(31), 7133-7155. https://doi.org/10.1021/bi00483a001
  • Dill, K. A., & MacCallum, J. L. (2012). The protein-folding problem, 50 years on. Science, 338(6110), 1042-1046. https://doi.org/10.1126/science.1219021
  • Eisenberg, D. (2003). The discovery of the α-helix and β-sheet, the principal structural features of proteins. Proceedings of the National Academy of Sciences, 100(20), 11207-11210. https://doi.org/10.1073/pnas.2034522100
  • Ernst, J. A., Clubb, R. T., Zhou, H. X., Gronenborn, A. M., & Clore, G. M. (1995). Demonstration of positionally disordered water within a protein hydrophobic cavity by NMR. Science, 267(5205), 1813-1817. https://doi.org/10.1126/science.7892604
  • Finney, J. L. (1977). The organization and function of water in protein crystals. Philosophical Transactions of the Royal Society of London. B, Biological Sciences, 278(959), 3-32. https://doi.org/10.1098/rstb.1977.0029
  • Fleming, P. J., Gong, H., & Rose, G. D. (2006). Secondary structure determines protein topology. Protein Science, 15(8), 1829-1834. https://doi.org/10.1110/ps.062305106
  • Flower, D. R., North, A. C., & Sansom, C. E. (2000). The lipocalin protein family: structural and sequence overview. Biochimica et Biophysica Acta (BBA)-Protein Structure and Molecular Enzymology, 1482(1-2), 9-24. https://doi.org/10.1016/S0167-4838(00)00148-5
  • Gupta, P. S. S., Banerjee, S., Islam, R. N. U., Mondal, S., Mondal, B., & Bandyopadhyay, A. K. (2014a). PHYSICO: An UNIX based Standalone Procedure for Computation of Individual and Group Properties of Protein Sequences. Bioinformation, 10(2), 105. https://doi.org/10.6026/97320630010105
  • Gupta, P. S. S., Mondal, S., Mondal, B., Islam, R. N. U., Banerjee, S., & Bandyopadhyay, A. K. (2014b). SBION: A program for analyses of salt-bridges from multiple structure files. Bioinformation, 10(3), 164. https://doi.org/10.6026/97320630010164
  • Gupta, P. S. S., Nayek, A., Banerjee, S., Seth, P., Das, S., Sur, V. P., … & Bandyopadhyay, A. K. (2015). SBION2: Analyses of salt bridges from multiple structure files, version 2. Bioinformation, 11(1), 39. https://doi.org/10.6026/97320630011039
  • Gutheil, W. G., Holmquist, B., & Vallee, B. L. (1992). Purification, characterization, and partial sequence of the glutathione-dependent formaldehyde dehydrogenase from Escherichia coli: a class III alcohol dehydrogenase. Biochemistry, 31(2), 475-481. https://doi.org/10.1021/bi00117a025
  • Islam, R. N. U., Mitra, D., Gupta, P. S. S., Banerjee, S., Mondal, B., & Bandyopadhyay, A. K. (2018). AUTOMINv1. 0: an automation for minimization of Protein Data Bank files and its usage. Bioinformation, 14(9), 525. https://doi.org/10.6026/97320630014525
  • Islam, R. N. U., Roy, C., Gupta, P. S. S., Banerjee, S., Mitra, D., Banerjee, S., & Bandyopadhyay, A. K. (2018). PROPAB: Computation of Propensities and Other Properties from Segments of 3D structure of Proteins. Bioinformation, 14(5), 190. https://doi.org/10.6026/97320630014190
  • Islam, R. N. U., Roy, C., Mitra, D., Bandyopadhyay, A. K., Yasmeen, S., & Banerjee, S. (2019). Salt-bridge, aromatic-aromatic, cation-π and anion-π interactions in proteins from different domains of life. In Biotechnology and Biological Sciences (pp. 152-158). CRC Press. https://doi.org/10.1201/9781003001614-25
  • Kendrew, J. C., Bodo, G., Dintzis, H. M., Parrish, R. G., Wyckoff, H., & Phillips, D. C. (1958). A three-dimensional model of the myoglobin molecule obtained by x-ray analysis. Nature, 181(4610), 662-666. https://doi.org/10.1038/181662a0
  • Kyte, J., & Doolittle, R. F. (1982). A simple method for displaying the hydropathic character of a protein. Journal of Molecular Biology, 157(1), 105-132. https://doi.org/10.1016/0022-2836(82)90515-0
  • Lim, V. I. (1974). Structural principles of the globular organization of protein chains. A stereochemical theory of globular protein secondary structure. Journal of Molecular Biology, 88(4), 857-872. https://doi.org/10.1016/0022-2836(74)90404-5
  • Lins, L., Thomas, A., & Brasseur, R. (2003). Analysis of accessible surface of residues in proteins. Protein Science, 12(7), 1406-1417. https://doi.org/10.1110/ps.0304803
  • Madern, D. (2002). Molecular evolution within the L-malate and L-lactate dehydrogenase super-family. Journal of molecular evolution, 54(6), 825-840. https://doi.org/10.1007/s00239-001-0088-8
  • Martinez, C. R., & Iverson, B. L. (2012). Rethinking the term “pi-stacking”. Chemical Science, 3(7), 2191-2201. https://doi.org/10.1039/c2sc20045g
  • Mecozzi, S., West Jr, A. P., & Dougherty, D. A. (1996). Cation-pi interactions in aromatics of biological and medicinal interest: electrostatic potential surfaces as a useful qualitative guide. Proceedings of the National Academy of Sciences, 93(20), 10566-10571. https://doi.org/10.1073/pnas.93.20.10566
  • Mitra, D., Bandyopadhyay, A. K., Islam, R. N. U., Banerjee, S., Yasmeen, S., & Mohapatra, P. K. D. (2019). Structure, salt-bridge’s energetics and microenvironments of nucleoside diphosphate kinase from halophilic, thermophilic and mesophilic microbes. In Biotechnology and Biological Sciences (pp. 107-113). CRC Press. https://doi.org/10.1201/9781003001614-18
  • Moon, J. H., Lee, H. J., Park, S. Y., Song, J. M., Park, M. Y., Park, H. M., … & Kim, J. S. (2011). Structures of iron-dependent alcohol dehydrogenase 2 from Zymomonas mobilis ZM4 with and without NAD+ cofactor. Journal of molecular biology, 407(3), 413-424. https://doi.org/10.1016/j.jmb.2011.01.045
  • Nayek, A., Banerjee, S., Sen Gupta, P. S., Sur, B. P., Seth, P., Das, S., … & Bandyopadhyay, A. K. (2015). ADSETMEAS: Automated determination of salt-bridge energy terms and micro environment from atomic structures using APBS method, version 1.0. In Protein Science, 24, 216-217. 111 RIVER ST, HOBOKEN 07030-5774, NJ USA: WILEY-BLACKWELL.
  • Nayek, A., Gupta, P. S. S., Banerjee, S., Sur, V. P., Seth, P., Das, S., … & Bandyopadhyay, A. K. (2015b). ADSBET2: Automated determination of salt-bridge energy-terms version 2. Bioinformation, 11(8), 413. https://doi.org/10.6026/97320630011413
  • Nayek, A., Gupta, P. S., Banerjee, S., Das, S., Sur, V. P., Seth, P., … & Bandyopadhyay, A. K. (2015a). ADSBET: Automated determination of salt-bridge energy terms. Int. J. Inst. Pharm. Life Sci., 5, 28-36.
  • Nayek, A., Sen Gupta, P. S., Banerjee, S., Mondal, B., & Bandyopadhyay, A. K. (2014). Salt-bridge energetics in halophilic proteins. Plos One, 9(4), e93862. https://doi.org/10.1371/journal.pone.0093862
  • Nayek, A., Sen Gupta, P. S., Banerjee, S., Mondal, B., & Bandyopadhyay, A. K. (2014). Salt-bridge energetics in halophilic proteins. Plos one, 9(4), e93862. https://doi.org/10.1371/journal.pone.0093862
  • Petitjean, C., Deschamps, P., López-García, P., & Moreira, D. (2015). Rooting the Domain Archaea by Phylogenomic Analysis Supports the Foundation of the New Kingdom Proteoarchaeota, Genome Biology and Evolution, 7(1), 191–204. https://doi.org/10.1093/gbe/evu274
  • Rose, G. D., Geselowitz, A. R., Lesser, G. J., Lee, R. H., & Zehfus, M. H. (1985). Hydrophobicity of amino acid residues in globular proteins. Science, 229(4716), 834-838. https://doi.org/10.1126/science.4023714
  • Rovers, E., & Schapira, M. (2022). Methods for computer-assisted PROTAC design. Methods in Enzymology, 690, 311-340. https://doi.org/10.1016/bs.mie.2023.06.020
  • Roy, C., Islam, R. N. U., Banerjee, S., & Bandyopadhyay, A. K. (2023). Underlying features for the enhanced electrostatic strength of the extremophilic malate dehydrogenase interface salt-bridge compared to the mesophilic one. Journal of Biomolecular Structure and Dynamics, 1-16. https://doi.org/10.1080/07391102.2023.2295972
  • Sadqi, M., Lapidus, L. J., & Munoz, V. (2003). How fast is protein hydrophobic collapse? Proceedings of the National Academy of Sciences, 100(21), 12117-12122. https://doi.org/10.1073/pnas.2033863100
  • Sen Gupta, P., Islam, R.N.U., Yasmeen, S. (2017). Cosurim: A program for automated computation of composition of core, rim and surface of protein data bank files and its applications. International Journal of Engineering Science and Technology, 9(11), 993-999.
  • Song, S. Y., Xu, Y. B., Lin, Z. J., & Tsou, C. L. (1999). Structure of active site carboxymethylated D-glyceraldehyde-3-phosphate dehydrogenase from Palinurus versicolor. Journal of Molecular Biology, 287(4), 719-725. https://doi.org/10.1006/jmbi.1999.2628
  • Song, S. Y., Xu, Y. B., Lin, Z. J., & Tsou, C. L. (1999). Structure of active site carboxymethylated D-glyceraldehyde-3-phosphate dehydrogenase from Palinurus versicolor. Journal of Molecular Biology, 287(4), 719-725. https://doi.org/10.1006/jmbi.1999.2628
  • Soukri, A., Mougin, A., Corbier, C., Wonacott, A., Branlant, C., & Branlant, G. (1989). Role of the histidine 176 residue in glyceraldehyde-3-phosphate dehydrogenase as probed by site-directed mutagenesis. Biochemistry, 28(6), 2586-2592. https://doi.org/10.1021/bi00432a036
  • Stollar, E. J., & Smith, D. P. (2020). Uncovering protein structure. Essays in Biochemistry, 64(4), 649–680. https://doi.org/10.1042/ebc20190042
  • Surti, M., Patel, M., Adnan, M., Moin, A., Ashraf, S. A., Siddiqui, A. J., … & Reddy, M. N. (2020). Ilimaquinone (marine sponge metabolite) as a novel inhibitor of SARS-CoV-2 key target proteins in comparison with suggested COVID-19 drugs: designing, docking and molecular dynamics simulation study. RSC Advances, 10(62), 37707-37720. https://doi.org/10.1039/D0RA06379G
  • Trevino, S. R., Scholtz, J. M., & Pace, C. N. (2007). Amino acid contribution to protein solubility: Asp, Glu, and Ser contribute more favorably than the other hydrophilic amino acids in RNase Sa. Journal of Molecular Biology, 366(2), 449-460. https://doi.org/10.1016/j.jmb.2006.10.026
  • Tsodikov, O. V., Record Jr, M. T., & Sergeev, Y. V. (2002). Novel computer program for fast exact calculation of accessible and molecular surface areas and average surface curvature. Journal of Computational Chemistry, 23(6), 600-609. https://doi.org/10.1002/jcc.10061
  • Williams, R. W., Chang, A., Juretić, D., & Loughran, S. (1987). Secondary structure predictions and medium range interactions. Biochimica et Biophysica Acta (BBA)-Protein Structure and Molecular Enzymology, 916(2), 200-204. https://doi.org/10.1016/0167-4838(87)90109-9
  • Williamson, V. M., & Paquin, C. E. (1987). Homology of Saccharomyces cerevisiae ADH4 to an iron-activated alcohol dehydrogenase from Zymomonas mobilis. Molecular and General Genetics MGG, 209, 374-381. https://doi.org/10.1007/BF00329668
  • Xiao, Y., Wu, K., Batool, S.S., Wang, Q., Chen, H., Zhai, X., Yu, Z., & Huang, J. (2023). Enzymatic properties of alcohol dehydrogenase PedE_M.s. derived from Methylopila sp. M107 and its broad metal selectivity. Front. Microbiol., 14, 1191436. https://doi.org/10.3389/fmicb.2023.1191436
  • Zielenkiewicz, P., & Saenger, W. (1992). Residue solvent accessibilities in the unfolded polypeptide chain. Biophysical Journal, 63(6), 1483-1486. https://doi.org/10.1016/S0006-3495(92)81746-0
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Life as Basic Science: An Overview and Prospects for Future [Volume: 3]

How to Cite
Amal Kumar Bandyopadhyay, Sahini Banerjee and Somnath Das (2024). Discovery of rim region between core and surface of proteins. © International Academic Publishing House (IAPH), Dr. Somnath Das, Dr. Jayanta Kumar Das, Dr. Mayur Doke and Dr. Vincent Avecilla (eds.), Life as Basic Science: An Overview and Prospects for the Future Volume: 3,pp. 41-96. ISBN: 978-81-978955-7-9
DOI: https://doi.org/10.52756/lbsopf.2024.e03.003

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